Bet hedging buffers budding yeast against environmental instability

Abstract

To grow and divide, cells must extract resources from dynamic and unpredictable environments. Organisms thus possess redundant metabolic pathways for distinct contexts. In budding yeast, ATP can be produced from carbon by mechanisms that prioritize either speed (fermentation) or yield (respiration). We find that in the absence of predictive cues, cells vary in their intrinsic ability to switch metabolic strategies from fermentation to respiration. We observe subpopulations of yeast cells which either rapidly adapt or enter a shock state characterized by deformation of many cellular structures, including mitochondria. This capacity to adapt is a bimodal and heritable state. We demonstrate that metabolic preparedness confers a fitness advantage during an environmental shift but is costly in a constant, high-glucose environment, and we observe natural variation in the frequency of prepared cells across wild yeast strains. These experiments suggest that bet-hedging has evolved in budding yeast.